Maintenance of Fungal Pathogen Species That Are Specialized to Different Hosts: Allopatric Divergence and Introgression through Secondary Contact

Sympatry of species that lack complete prezygotic isolation is ideal for the study of how species can be maintained in the face of potential gene flow. This is particularly important in the context of emerging diseases on new hosts because pathogen adaptation is facilitated by reduced gene flow from ancestral populations. Here, we investigated divergence and gene flow between two closely related fungal species, Microbotryum lychnidis-dioicae and M. silenes-dioicae, causing anther-smut disease on the wide-spread plant species Silene latifolia and S. dioica, respectively. Using model-based clustering algorithms on microsatellite data from samples across Europe, we identified rare disease transmission between the host species and rare pathogen hybrids. Using a coalescent-based approach and an isolation-with-migration model, the age of divergence between the two fungal species was estimated at approximately 4.2 x 10(5) years. Levels of gene flow were low and concentrated in very recent times. In addition, gene flow appeared unidirectional from M. silenes-dioicae to M. lychnidis-dioicae. Altogether, our findings are consistent with a scenario of recurrent introgressive hybridization but at a very low level and through secondary contact following initial divergence in allopatry. Asymmetry in the direction of gene flow mirrors previous findings on introgression between the two host plants. Our study highlights the consequences of bringing closely related pathogens into contact, which is increasing through modern global changes and favors cross-species disease transmission, hybridization, and introgression by pathogens.